MicroRNA 203 Modulates Glioma Cell Migration via Robo1/ERK/MMP-9 Signaling

Genes and Cancer

Volumn 4, Issue 7-8, 2013, Pages 285-296

  Dontula, Ranadheer ^a   Dinasarapu, Ashok ^b   Chetty, Chandramu ^c   Pannuru, Padmavathi ^a   Herbert, Engelhard ^c   Ozer, Howard ^a   Lakka, Sajani S ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

cell migration; glioma; invasion; miR 203; Robo1

Indexed keywords

GELATINASE B; LUCIFERASE; MICRORNA; MICRORNA 203; MITOGEN ACTIVATED PROTEIN KINASE; PLASMID VECTOR; ROUNDABOUT 1 RECEPTOR; ROUNDABOUT RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER GRADING; CANCER INHIBITION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; GENE EXPRESSION; GENE FUNCTION; GLIOBLASTOMA; GLIOMA CELL; IN SITU HYBRIDIZATION; MIGRATION INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA GENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WESTERN BLOTTING;

EID: 84887478941     PISSN: 19476019     EISSN: 19476027     Source Type: Journal    
DOI: 10.1177/1947601913500141     Document Type: Article

References (50)

1. Ohgaki H,Kleihues P.Epidemiology and etiology of gliomas.Acta Neuropathol. 2005;109 (1): 93-108.
2. Grauer OM,Wesseling P,Adema GJ.Immunotherapy of diffuse gliomas: biological background, current status and future development.Brain Pathol. 2009;19 (4): 674-93.
3. Parsons DW,Jones S,Zhang X,et al.An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321 (5897): 1807-12.
4. Volinia S,Calin GA,Liu CG,et al.A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006;103 (7): 2257-61.
5. Esquela-Kerscher A,Slack FJ.Oncomirs-microRNAs with a role in cancer.Nat Rev Cancer. 2006;6 (4): 259-69.
6. He L,Hannon GJ.MicroRNAs: small RNAs with a big role in gene regulation.Nat Rev Genet. 2004;5 (7): 522-31.
7. Ambrose V.microRNAs: tiny regulators with great potential.Cell. 2001;107 (7): 823-6.
8. Bartel DP.MicroRNAs: genomics, biogenesis, mechanism, and function.Cell. 2004;116 (2): 281-97.
9. Eulalio A,Huntzinger E,Izaurralde E.Getting to the root of miRNA-mediated gene silencing.Cell. 2008;132 (1): 9-14.
10. Lee RC,Feinbaum RL,Ambros V.The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14.Cell. 1993;75 (5): 843-54.
11. Zhang L,Huang J,Yang N,et al.microRNAs exhibit high frequency genomic alterations in human cancer.Proc Natl Acad Sci U S A. 2006;103 (24): 9136-41.
12. Fazi F,Racanicchi S,Zardo G,et al.Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein.Cancer Cell. 2007;12 (5): 457-66.
13. Hammond SM.MicroRNAs as tumor suppressors.Nat Genet. 2007;39 (5): 582-3.
14. Hiyoshi Y,Kamohara H,Karashima R,et al.MicroRNA-21 regulates the proliferation and invasion in esophageal squamous cell carcinoma.Clin Cancer Res. 2009;15:1915-22.
15. Ma J,Dong C,Ji C.MicroRNA and drug resistance.Cancer Gene Ther. 2010;17:523-31.
16. Ma L,Teruya-Feldstein J,Weinberg RA.Tumour invasion and metastasis initiated by microRNA-10b in breast cancer.Nature. 2007;449 (7163): 682-9.
17. Nicoloso MS,Spizzo R,Shimizu M,Rossi S,Calin GA.MicroRNAs-the micro steering wheel of tumour metastases.Nat Rev Cancer. 2009;9 (4): 293-302.
18. Shenouda SK,Alahari SK.MicroRNA function in cancer: oncogene or a tumor suppressor?.Cancer Metastasis Rev. 2009;28 (3-4): 369-78.
19. Dichamp C,Taillibert S,Aguirre-Cruz L,et al.Loss of 14q chromosome in oligodendroglial and astrocytic tumors.J Neurooncol. 2004;67 (3): 281-5.
20. Hu J,Jiang C,Ng HK,Pang JC,Tong CY,Chen S.Genome-wide allelotype study of primary glioblastoma multiforme.Chin Med J (Engl). 2003;116 (4): 577-83.
21. Liang P,Pardee AB.Analysing differential gene expression in cancer.Nat Rev Cancer. 2003;3 (11): 869-76.
22. McLendon R,Friedman A,Bigner D,et al.Comprehensive genomic characterization defines human glioblastoma genes and core pathways.Nature. 2008;455 (7216): 1061-8.
23. Dong H,Luo L,Hong S,et al.Integrated analysis of mutations, miRNA and mRNA expression in glioblasoma.BMC Syst Biol. 2010;4:163.
24. Legg JA,Herbert JM,Clissold P,Bicknell R.Slits and roundabouts in cancer, tumor angiogenesis and endothelial cell migration.Angiogenesis. 2008;1 (1): 13-21.
25. Wiedemeyer R,Brennan C,Heffernan TP,et al.Feedback circuit among INK4 tumor suppressors constrains human glioblastoma development.Cancer Cell. 2008;13 (4): 355-64.
26. Murat A,Migliavacca E,Gorlia T,et al.Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma.J Clin Oncol. 2008;26 (18): 3015-24.
27. Borchert GM,Lanier W,Davidson BL.RNA polymerase III transcribes human microRNAs.Nat Struct Mol Biol. 2006;13 (12): 1097-101.
28. Huang C,Jacobson K,Schaller MD.MAP kinases and cell migration.J Cell Sci. 2004;117 (Pt 20): 4619-28.
29. Zhang B,Pan X,Cobb GP,Anderson TA.microRNAs as oncogenes and tumor supressors.Dev Biol. 2007;302 (1): 1-12.
30. Valastyan S,Weinberg RA.Assaying microRNA loss-of-function phenotypes in mammalian cells: emerging tools and their potential therapeutic utility.RNA Biol. 2009;6 (5): 541-5.
31. Lagana A,Russo F,Sismeiro C,Giugno R,Pulvirenti A,Ferro A.Variability in the incidence of miRNAs and genes in fragile sites and the role of repeats and CpG islands in the distribution of genetic material.PLoS One. 2010;5 (6): e11166.
32. Boll K,Reiche K,Kasack K,et al.MiR-130a, miR-203 and miR-205 jointly repress key oncogenic pathways and are downregulated in prostate carcinoma.Oncogene. 2013;32 (3): 277-85.
33. Bian K,Fan J,Zhang X,et al.MicroRNA-203 leads to G1 phase cell cycle arrest in laryngeal carcinoma cells by directly targeting survivin.FEBS Lett. 2012;586 (6): 804-9.
34. Wang C,Zheng X,Shen C,Shi Y.MicroRNA-203 supresses cell proliferation and migration by targeting BIRC5 and LASP1 in human triple-negative breast cancer cells.J Exp Clin Cancer Res. 2012;31:58.
35. Simpson JH,Kidd T,Bland KS,Goodman CS.Short-range and long-range guidance by slit and its Robo receptors. Robo and Robo2 play distinct roles in midline guidance.Neuron. 2000;28 (3): 753-66.
36. Wang LJ,Zhao Y,Han B,et al.Targeting Slit-Roundabout signaling inhibits tumor angiogenesis in chemical-induced squamous cell carcinogenesis.Cancer Sci. 2008;99 (3): 510-17.
37. Zhou WJ,Geng ZH,Chi S,et al.Slit-Robo signaling induces malignant transformation through Hakai-mediated E-cadherin degradation during colorectal epithelial cell carcinogenesis.Cell Res. 2011;21 (4): 609-26.
38. Roberts PJ,Der CJ.Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer.Oncogene. 2007;26 (22): 3291-310.
39. Neill GW,Harrison WJ,Ikram MS,et al.GLI1 repression of ERK activity correlates with colony formation and impaired migration in human epidermal kertinocyte.Carcinogenesis. 2008;29 (4): 738-46.
40. Kessenbrock K,Plaks V,Werb Z.Matrix metalloproteinases: regulators of the tumor microenvironment.Cell. 2010;141 (1): 52-67.
41. Wang M,Wang T,Liu S,Yoshida D,Teramoto A.The expression of matrix metalloproteinase-2 and -9 in human gliomas of different pathological grades.Brain Tumor Pathol. 2003;20 (2): 65-72.
42. Glassmann A,Reichmann K,Scheffler B,Glas M,Veit N,Probstmeier R.Pharmacological targeting of the constitutively activated MEK/MAPK-dependent signaling pathway in glioma cell inhibits cell proliferation and migration.Int J Oncol. 2011;39 (6): 1567-75.
43. Saini S,Majid S,Yamamura S,et al.Regulatory role of mir-203 in prostate cancer progression and metastasis.Clin Cancer Res. 2011;17 (16): 5287-98.
44. Yi R,Poy MN,Stoffel M,Fuchs E.A skin microRNA promotes differentiation by repressing "stemness.".Nature. 2008;452:225-9.
45. Lena AM,Shalom-Feuerstein R,Rivetti di Val Cervo P,et al.miR-203 represses "stemness" by repressing DeltaNp63.Cell Death Differ. 2008;15 (7): 1187-95.
46. Wellner U,Schubert J,Burk UC,et al.The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs.Nat Cell Biol. 2009;11 (12): 1487-95.
47. Abella V,Valladares M,Rodriguez T,et al.miR-203 regulates cell proliferation through its influence on Hakai expression.PLoS One. 2012;7 (12): e52568.
48. Giannini C,Sarkaria JN,Saito A,et al.Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme.Neuro Oncol. 2005;7:164-76.
49. Gondi CS,Lakka SS,Dinh DH,Olivero WC,Gujrati M,Rao JS.Downregulation of uPA, uPAR and MMP-9 using small, interfereing, hairpin RNA (siRNA) inhibits glioma cell invasion, angiogenesis and tumor growth.Neuron Glia Biol. 2004;1 (2): 165-76.
50. Rao CN,Lakka SS,Kin Y,et al.Expression of tissue factor pathway inhibitor 2 inversely correlates during the progression of human gliomas.Clin Cancer Res. 2001;7 (3): 570-6.